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Swimming asleep: characterization, ontogenesis and energetic basis of sleep during paddling in waterfowl

Periodic Reporting for period 1 - SLEEPSWIM (Swimming asleep: characterization, ontogenesis and energetic basis of sleep during paddling in waterfowl)

Reporting period: 2021-04-01 to 2023-03-31

Sleep is a common behavior among animals, but its purpose is not fully understood. Despite sleep usually being characterized by quiescence, some animals need to both sleep and move simultaneously. To mitigate this conflict, a unique state in which one brain hemisphere is awake while the other sleeps has evolved in some taxonomic groups. During such unihemispheric sleep, the eye opposite the awake hemisphere is open while the other is closed. Dolphins and fur seals rely on unihemispheric sleep to swim and watch for predators. Birds can also sleep unihemispherically, but it is unclear whether they can sleep while actively moving. Although frigatebirds can sleep during passive flight modes, sleep during flapping flight has not been observed. Given the technical challenges of studying sleep during active flight, we used an alternative approach to investigate whether birds can sleep during active locomotion. This approach was inspired by field observations of geese apparently swimming with at least one eye closed. Here, using video and accelerometry, we investigate "sleep-swimming" in captive juvenile Canada geese imprinted to follow us. We found that Canada geese can actively paddle their feet while asleep with one or both eyes closed. However, there was no relationship between which eye was closed and which foot was paddling, suggesting that sleep and paddling are controlled independently. Sleep-swimming increased with distance swam and decreased with age. Thus, geese seem to employ sleep-swimming when they are energetically challenged and/or the homeostatic pressure to sleep is elevated. By demonstrating that sleep and active locomotion are compatible, our findings suggest that sleep might also be possible during continuous flapping flight in migratory birds.
The current project lasted two years, from April 2021 until March 2023. The activities carried out during this period can be divided into three main groups: egg collection and gosling hand-raising, data collection, and data analysis. These phases alternated throughout the duration of the project.

The egg collection and gosling hand-raising phase took place in spring (March - June). To investigate ontogeny, we used two different cohorts of goslings, one in 2021 and another in 2022. During the first two spring months, my colleagues and I monitored the areas surrounding the institute and mapped the presence of nesting pairs of Canada geese. Once found, the nests were regularly monitored until the eggs were laid, at which point we collected them and incubated them at the institute until hatching. The newborn goslings were then hand-raised and imprinted on the experimenters, which allowed them to be naturally motivated to participate in the experimental sessions.

Between June and November, we conducted a data collection and analysis phase, which involved regular experimental sessions with the geese. During these sessions, the geese swam multiple laps along the length of the floating aviary following our inflatable boat, while we collected video and accelerometer data to investigate sleep-swimming in a gradient of increased workload, as well as the physiological need for sleep. Several experimental sessions were conducted across the entire period in order to investigate how the occurrence of sleep-swimming varies across development. We also collected continuous 24-hour data on undisturbed animals either before or after each experimental session to study sleep-swimming in a more natural context. Once the geese's skulls reached an adult-like size, we mounted a small logger that allowed us to confirm electrophysiologically whether the closing of the eyes indicated sleep. To analyze the vast amount of data, I automated the video analysis and extracted paddling data from the accelerometer data, with guidance from Dr. Paul Antoine Libourel (CRNL, SLEEP Team, Université Claude Bernard Lyon 1, France) whom I visited twice for training on this type of analysis on MATLAB.

Our preliminary findings indicate that Canada geese can actively move their legs while their eyes are closed, with a higher occurrence of sleep-swimming with both eyes closed when the distance swam increased. Moreover, we observed an increase in the total amount of sleep-swimming across the number of trips swam. This finding suggests that geese use sleep-swimming to meet an increased need for sleep, indicating an important role of this behavior in maintaining sleep homeostasis and potentially managing energy during movements within their habitat. Finally, our preliminary results show a decrease in the occurrence of sleep-swimming that correlates with the individual's growth, further suggesting a correlation between energy demand and sleep pressure. While conclusive results require further data analysis, our EEG data confirms that geese can sleep while actively swimming. Based on this, I am pleased to report that the objectives of this project have been achieved.
Throughout the project, I actively promoted it to both academic and non-academic audiences, including participating in the MPI-BI open-day, featuring in two documentaries (one of which was aired on German TV), being interviewed by the Italian TV show Newton, delivering a seminar at the Italian Society of Ethology, speaking at a workshop organized by the University of Vienna, and having an article published about our project in a local newspaper. Although preliminary results have only recently been obtained, they will be disseminated next summer through my participation in two conferences: the European Ornithological Union Meeting 2023 and Behavior 2023. Additionally, I kept important milestones visible on social media platforms like Facebook and Twitter.
We found that birds can move their legs in a coordinated manner while sleeping, which is a significant discovery in sleep research. Previously, this phenomenon has only been observed in aquatic mammals. While the results are still preliminary, as only a small portion of the videos have been analyzed, we expect to complete the analysis in 6-12 months. I plan to publish at least two papers on this topic in a high-ranking journal, given the innovation and impact of these findings.

This project expanded our understanding of stereotyped movements during sleep in birds, and their relationship with ecological demands. Innovative methods were used, including working with captive birds in a seminatural setting and advanced recording techniques. The investigation of sleep-swimming has opened new possibilities for studying sleep during endurance flights and similar phenomena in other species. For example, sleep-swimming could also be used as a model for investigating sleep-walking in humans, a dangerous condition for which no animal models exist. The data gathered through less invasive techniques demonstrated their reliability in measuring sleep, which can reduce the need for invasive methods in future sleep studies. Sleep-swimming has also been shown to be an indicator of environmental disturbance and/or increased energy demand, which can be useful for conservation purposes.
Example of synched eye state detection and leg accelerometer data showing sleep-swimming